Open access journal: http://periodicos.uefs.br/ojs/index.php/sociobiologyISSN: 0361-6525

DOI: 10.13102/sociobiology.v60i3.337-344Sociobiology 60(3): 337-344 (2013)

Social Wasp-Flower Visiing Guild Interacions in Less Structurally Complex Habitats are More Suscepible to Local Exincion

MA Clemente1, D Lange2, W Dáttilo3, K Del-Claro2, F Prezoto4

Introduction

The importance of species interactions for the mainten-ance of biodiversity has been widely recognized (Thompson, 2013; Del-Claro & Torezan-Silingardi, 2009). These interac-tions vary from mutualistic to antagonistic and affect popula-tions and individuals in different ways, since all species es-tablish ecological interaction at some point in their lifetime. It is also recognized that ecological interactions vary in time and space (Thompson, 2013; Del-Claro et al., 2013) and that structurally more heterogeneous and complex environments have a higher species richness and diversity. Alternatively, more homogeneous environments are simpler in their struc-ture and less diverse (Santos et al., 2007; Tews et al., 2004).

Currently, network analysis has been widely used for ecological interaction studies. This tool enables conclusions concerning the structure, stability and robustness of ecologi-

Abstract

Several studies have shown that habitat complexity is an important factor for the dy-namic and stability of interacing species. However, it is not known how the habitat complexity may afect the tolerance of wasp-lower interacions to local exincion. Based on this perspecive, in this study, we aimed to compare the tolerance of wasp lower visiing guild to local exincion in two diferent types of vegetaion (Riparian For-est and Rocky Grassland). Through observaions made during one year, we veriied that the structure of the plant-wasp interacion network difered between the two areas, as well as that the robustness to cumulaive exincions had diferent paterns. The simulaions of cumulaive removal of species showed that the network in the Riparian Forest is more robust against the removal of both plants and wasps than that network in Rocky Grassland, since their exincion curves declined more slowly. Therefore, in our study area, we demonstrate that social wasp-plant interacions in areas with lower structural complexity are less tolerant to exincion (i.e. more fragile). We therefore suggest that studies that aim at biodiversity conservaion should focus not only in areas where diversity is high, but also in area with lower species richness for the conservaion of ecological roles within communiies.

SociobiologyAn international journal on social insects

1 - Universidade Estadual Paulista, Rio Claro, São Paulo, Brazil

2 - Universidade Federal de Uberlândia, Uberlândia, Minas Gerais, Brazil

3 - Universidad Veracruzana, Xalapa, Veracruz, Mexico

4 - Universidade Federal de Juiz de Fora. Juiz de Fora, Minas Gerais, Brazil

Aricle HistoryEdited byGilberto M M Santos, UEFS, BrazilReceived 08 June 2013Iniial acceptance 12 July 2013Final acceptance 26 July 2013

KeywordsEcological networks, lower-visiing, species loss, habitat complexity, robustness

Corresponding authorDenise LangeLab. de Ecologia Comportamental e Interações - Insituto de BiologiaUniversidade Federal de UberlândiaUberlândia, Minas Gerais, CP 59338400-058, Brazil E-Mail: deniselange@yahoo.com.br

cal interactions involving two or more groups of organisms to be reached (Montoya et al., 2006; Thébault & Fontaine, 2010; Hernández-Yáñez et al., 2013). Our current understanding about how ecological networks might have different patterns in distinct habitats has, in general, been limited to few studies (see Clemente et al., 2012; Dáttilo et al., 2013a). From this, we can infer that structurally different habitats might have dif-ferent patterns of ecological networks and consequently vary in their tolerance to species loss.

Studies on species extinction have been the focus of conservation ecologists who aim to preserve biodiversity, however, such studies approach only the loss of species, with-out considering the loss of the functional role that species exert (Memmott et al., 2007; Dyer et al., 2010). In natural systems, each species performs specialized functions or those complementary to its partners (Blüthgen & Klein, 2011). In interactions among species specialists (i.e. with a narrow

RESEARCH ARTICLE - WASPS

MA Clemente, D Lange, W Dáilo, K Del-Claro, F Prezoto - Exincion of an ecological interacion338

niche breadth), each species is extremely important for inter-active pair and the loss of one species results in the loss of the interaction and the extinction of one of its associates (Blüth-gen & Klein, 2011). Alternatively, the extinction of generalist species (i.e. with a wide niche), causes fewer effects on its associates, because complementary functions are provide by other species. However, regardless of the ecological function, the extinction of an interaction between two species can inlu-ence the structure of the ecological network within an entire community (Olesen & Jain, 1994).

According to Santos et al. (2007), interactions estab-lished among social wasps and plants (e.g. Torezan-Silingardi 2011) are a good system to study the issues of co-extinction in ecological networks and the effect of abiotic factors on them, since they have certain requirements from the environment, for example, the habitat might provide a nesting substrate (Santos & Gobbi, 1998; Cruz et al., 2006), food resources (e.g. nectar) (Santos et al., 1998; Silva-Pereira & Santos, 2006; Santos et al., 2006), material for nest building (e.g. plant iber) (Machado, 1982; Marques & Carvalho, 1993) and prey (Santos et al., 1998).

Thus, the loristic composition, vegetation structure and complexity are determinants of the composition and commu-nity structure of social wasps (Santos et al., 2007). Addition-ally, some wasp species build their nests only under speciic structural conditions of vegetation (Sinzato et al., 2011), which can be open or closed landscapes, as well as morphological conditions of the plant species; the size and shape of leaves, stem diameter and/or the presence of thorns (Henriques et al., 1992; Santos & Gobbi, 1998; Cruz et al., 2006). Thus, the complexity of the vegetation is determinant for the composi-tion and community structure of social wasps and its funda-mental and realized niche (Santos et al., 2007; Carvalho et al., 2013). Therefore, environments with different complexities of vegetation might hypothetically have interaction networks with different compositions and topological properties, and consequently have different degrees of tolerance to species extinction. In this study, we compared the tolerance of the interaction network between lower-visiting social wasps and plants to extinction, in two distinct areas with different types of vegetation in the Brazilian Savanna (Riparian Forest and Rocky Grassland), to analyze in which vegetation physiog-nomy the wasp-plant interactions are more fragile.

Materials and Methods

We collected data in the Parque Estadual do Ibitipoca (Unidade de Conservação) (PEIB - 21º40’44”S and 43º52’55”W), southeastern Brazil, from November 2007 to October 2008. The PEIB is managed by the Forestry Institute, organ of the En-vironment Agency of the State of Minas Gerais. Moreover, the area is composed of several vegetation types that form different phytophysiognomies. Riparian Forest and Rocky

Grassland are the most abundant phytophysiognomies of the PEIB. The Riparian Forest exhibits a proile of transition ve-getation from high-altitude savannas to ombrophilous forests, with a physiognomy sequence from shrubby-arboreal to pre-dominantly arboreal and a great heterogeneity of plant species (Durigan et al., 2000), with a predominance of cloudiness (i.e. high moisture) (Fontes, 1997). The Rocky Grassland exhibits a xeromorphic aspect, with a wide diversity of herbs and shrubs distributed over quartzite outcrops (Rodela, 1998). This area is dominated by plants tolerant to water stress, due to the high incidence of light and wind (Giulietti et al., 1997).

At each of the two studied sites, which were 1,200 m

distant from each other, we used one transect of 800 x 4 m,

where we carried out monthly observations on two consecu-

tive days between 7:00 - 17:00 h, during this period, we ob-

served each plant that had lowers for 10 min and collected one individual of each wasp species that visited the lowers. Capture was performed using entomological sweep net, ac-

cording to the method of Sakagami et al. (1967).

Data Analysis

Initially, we built two quantitative wasp-plant adjacency matrices (one for each vegetation type), c

ij =

number of interactions between wasp species i and plant species j inside in transects. In order not to overestimate the plant species with more number of lowers, we considered as interaction frequency only the interactions among individuals within transects. To test whether the composition of plants and wasps shifts along the core-periphery gradient of the networks in each area, we deined the core of generalist species according to Dáttilo et al. (2013b). The species that exhibit a Cp > 1 are species with a higher proportion of interactions in relation to other species of the same group and are therefore considered core species of the network. The species with a Cp < 1 are species with a lower proportion of interactions and are considered periphery species.

We calculated the robustness to extinction for both wasp-plant interaction networks (Riparian Forest and Rocky Grassland), based on the cumulative removal of species from the network at random (sensu Burgos et al., 2007; Dáttilo et al., 2012). We also calculated the area under the extinction curve (R) according to Burgos et al. (2007), as a measure of the robustness of the networks, which varied from 1.0 (a more robust network) to 0 (a less robust network).

We ran 100 randomizations for each network to simulate species removal and we chose the R index because it is more robust and is not sensitive to the shape of the curve, in contrast to the index proposed by Memmott et al. (2004). We used the Network 3D Software (Williams, 2010) to create the graphical representations of social wasp–plant networks, and the Attack Tolerance Curve (ATC) to calculate the R index.

Sociobiology 60(3): 337-344 (2013) 339

Results

In this study, we recorded 15 wasp species in associations with 27 plant species (or morphospecies) (Table 1). A list of all wasp–plant interactions recorded can be viewed in the supplementary material (Appendix 1). The social wasp-plant interaction networks of two Cerrado physiognomies showed different structure (Fig 1). The network in the Riparian Forest had a greater number of species (18 plant species and 15 wasp species) and a fourfold greater number amount of connections between them (83 associations) compared to the Rocky Grassland (11 plant species, eight wasp species, and 20 associations). The percentage of plant and wasp core species was also different between the two landscapes, with a greater number of wasp species belonging to the principal core in the Riparian Forest (16.6 % for plants and 20% for wasps in Riparian Forest, and 37.5% for plants and 9.1% for wasps in Rocky Grassland). The average degree of plant and wasp species was also different between areas (2.44 for plants and 2.93 for wasps in Riparian Forest, and 1.27 for plants and 1.75 for wasps in Rocky Grassland).

The robustness to cumulative extinctions showed dif-ferent pattern at each site (Fig 2). The simulations of the cu-mulative removal of species showed that the network in the Riparian Forest is more robust against the removal of both plants and wasps than the network in the Rocky Grassland, since their extinction curves declined more slowly. The ro-bustness of the network in the Riparian Forest was relatively high, both for plants (R = 0.914) and wasps (R = 0.706) (see Fig 2C, D). In the Rocky Grassland network, the robustness was lower for plants (R = 0.799) and wasps (R = 0.658) (see Fig 2A, B).

Discussion

Our results show that interactions between social wasps and lowers have a different tolerance to species extinction in habitats with a distinct vegetation structure. Furthermore, we showed that in the Brazilian Cerrado, a more heterogeneous habitat exhibit plant-social wasp networks that are more tole-rant to the extinction of interactions.

Table 1. Code of plant and wasp species exhibited in Figure 1.

Code Plant Species Code Wasp Species

MSE Mandevilla sellowii (Müll. Arg.) Woodson AMU Agelaia multipicta (Haliday, 1836)

DLA Ditassa laevis Mart. APA Apoica pallens (Fabricius, 1804)

AS1 Asteraceae sp1 BLE Brachygastra lecheguana (Latreille, 1824)

AS2 Asteraceae sp2 COM Mischocyttarus confusus Zikán, 1935

AS3 Asteraceae sp3 MDR Mischocyttarus drewseni Saussure, 1857

AS4 Asteraceae sp4 PBI Polistes billardieri Fabricius, 1804

AS5 Asteraceae sp5 PCI Polistes cinerascens Saussure, 1854

AS6 Asteraceae sp6 PFE Polistes ferreri Saussure, 1853

VE1 Vernonia sp1 PO1 Polistes sp1

BAC Baccharis sp1 PFF Polybia fastidiosuscula Saussure, 1854

VER Vanillosmopsis erythropappa (DC.) Sch. Bip. PIG Polybia ignobilis (Haliday, 1836)

WEI Weimmannia sp1 PPA Polybia paulista (Von. Ihering, 1896)

EGO Erythroxylum gonocladum (C. Martius) O. E. Schulz PSC Polybia sericea (Oliver, 1791)

PER Periandra sp1 PB1 Polybia sp1

CUP Cuphea sp1 PSY Protonectarina sylveirae (Saussure, 1854)

MEL Melastomataceae sp1

TPA Trembleya parvilora (D. Don) Cogn.

MFA Myrcia fallax (Rich.) DC

CCO Calyptranthes concinna DC.

OUR Ouratea sp1

PVE Prosthechea vespa (Sw.) W.E.Higgins

TSP Trachypogon spicatus (L. F.) Kuntze

PLA Posoqueria latifolia (Rudge) Schult.

BAR Barreria sp1

GFR Gordonia fruticosa (Schrad.) H. Keng

BFL Barbacenia lava Mart. ex Schult. F.

VAL Vellozia albilora Pohl

MA Clemente, D Lange, W Dáilo, K Del-Claro, F Prezoto - Exincion of an ecological interacion340

Vegetation complexity is positively related to spe-cies diversity in many groups of organisms (see Tews et al., 2004) including social wasps (see Lawton, 1983; Santos et al., 2000, 2007). According to Santos et al. (2007), vegetation is the main substrate for the foundation of social wasp nests, so more heterogeneous environments increase the quantity and variety of sites for nesting, and consequently, the coexistence of wasp species in these locations becomes greater.

In our study, this inding was conirmed in the Ripar-ian Forest, which showed the greatest number of wasp and plant species, number of associations and interaction degree between plant-wasp species. A greater complexity in forest than in grassland areas has also been demonstrated in other studies (see review in Tews et al., 2004).

Previous studies have shown that wasp-plant networks are highly generalists (Mello et al., 2011; Aguiar & Santos, 2007). Here, we show that that despite the generalization of these networks, this pattern can vary between habitats with different complexity. Environments with a greater avail-

ability of resources (food or nesting sites) have lower levels of species competition (Markwell et al., 1993; Harris et al., 1994), mainly among wasps, where the competition for loral resources is rare (De Souza et al., 2010). The lower competi-tion, or lack thereof, contributes to the increase in species co-existence and local biodiversity (Henriques et al., 1992; Bas-tolla et al., 2009). Although, the social interaction between wasps and lowers in the Riparian Forest is more generalist that in the Rocky Grassland, most wasp species of both net-works established an association with only one plant species. This result might relate to limitations in resource collection by wasps from plants with a speciic loral morphology (i.e. length corollas) (see Heithaus, 1979a), because the mouthpart of wasps is short. Several authors have suggested that this is one of the main factors limiting of the niche breadth in wasps (Heithaus, 1979a; Johnson & Steiner, 2000; Shuttleworth & Johnson, 2006).

Nectar is an important resource for Hymenoptera de-velopment and survivorship (e.g. Byk & Del-Claro, 2011), and despite nectar being considered an accessory food in the diet of wasps (Faegri & Van der Pijl, 1979), they tend to pref-erentially visit plants that produce higher amounts of nectar (Gess & Gess, 1993), which leads to an increase in the coex-istence between of wasp species in a particular plant species. Since the competition for food in wasps is rare (De Souza et al., 2010), this factor poorly explains the specialization in this interaction, because the specialization observed in this study might be explained by a low abundance and richness of wasps and not by the coevolution of the associates.

Fig 2. Robustness to cumulative species removal of plants (A) and wasps (B) in the Rocky Grassland, and plants (C) and wasps (D) in

the Riparian Forest network.

Fig 1. Graphical representation of social wasp–plant networks of two phytophysiognomies (A) Rocky Grassland and (B) Riparian Forest of a Brazilian Savanna in the period from November 2007 to October 2008. The red nodes represent different plant species, and the yellow nodes correspond to wasp species that interact with plants. Lines represent wasp–plant interactions. Plant and wasp spe-

cies codes are presented in Table 1.

Sociobiology 60(3): 337-344 (2013) 341

In addition to the aforementioned factors, abiotic com-ponents might also explain the variation in specialization of the social wasp-lower interaction. Some social wasp species such as euriecias have a wide ecological valence, nesting in every type of habitat (Wenzel, 1991; Marques & Carvalho, 1993; Santos & Gobbi, 1998). However, the species estenoe-

cias exhibits a narrow limit of ecological valence, only nest-ing in speciic locations (Silva-Pereira & Santos, 2006; Santos et al., 2007, Souza et al., 2010), which might result in local extinction as an outcome of variations in habitat conditions. For example, wasp species such as Angiopolybia pallens (Lepeletier, 1836) and Synoeca cyanea (Fabricius, 1775) are

only found in environments with speciic substrate condi-tions (Marques, 1996; Santos et al., 2007), whereas Polistes

canadensis (Linnaeus, 1758), and Polybia ignobilis (Haliday, 1836) can alter their nesting habits according to the available environmental conditions and substrates (Santos & Gobbi, 1998; Santos et al., 2007). Thus, the ecological valence of wasp species might inluence species diversity in an environ-ment and major change in its microclimate might cause the extinction or migration of species at higher rates than in an environment where climatic conditions are more stable (Wil-son, 1988).

The factors mentioned above might have been deci-sive in the differentiation of the specialization and variation in the tolerance to extinction of the species interaction in the social wasp-lower networks studied. The Rocky Grassland area, which has less dense vegetation with strong winds and a high light incidence, might experience a large variation in microclimates, which might have contributed to a lower spe-cies diversity in this area (see Elpino-Campos et al., 2007). Unlike the Riparian Forest, which has a greater availability of resources, species coexistence, and a more generalist social wasp-lower interaction network. In fact, the more generalist networks tend to be functionally redundant and more robust to species extinction (Dáttilo et al., 2012). Furthermore, the presence of trees in this area maintains the stability of the lo-cal microclimate, as shown by Hernandes et al. (2004).

The importance of interaction conservation between social wasps and lowers has been only recently recognized (Shuttleworth & Johnson, 2009), because wasps were previ-ously considered as thieves of loral resources (Hunt et al., 1991; Elpino-Campos et al., 2007). Recent studies have shown that some species can contribute to pollination (Sühs et al., 2009). According to Heithaus (1979a, b), the guild of wasps that visit lowers surpasses that of bees in terms of exploita-tion of nectar in various ecosystems. Some species, such as Polistes versicolor (Olivier, 1791), Polistes simillimus Zikán, 1951, Polybia sericea (Olivier, 1791), and Polybia ignobilis (Haliday, 1836), can be more representative in richness and abundance than bee species and are eficient pollinators (see Sühs et al., 2009). Despite that social wasp-plant interactions be considered as non-obligatory mutualistic associations and leans to generalization rather than to specialization (Santos et

al., 2010; Mello et al., 2011), as other interactions involving plants and pollinators (see Hernández-Yáñez et al., 2013), the extinction of this interaction might result in the loss of part of the ecological function of pollination and cause damages to the community (see Blüthgen & Klein, 2011), especially in environments where this interaction is more specialized (Olesen & Jain, 1994). In these cases, the extinction of a pol-linator (even an eventual pollinator) might trigger the loss of plant species and begin a ‘cascade of linked extinctions’ (My-ers, 1986).

Although studies containing greater number of net-works are needed to conirm these results, our data show that social wasp-lower interactions in areas with low structural complexity might be less tolerant to extinction, (i.e. they are more fragile). Thus, we suggest that studies that aim at bio-diversity conservation should focus not only on areas where diversity is high, but also in areas with lower species richness, because the dependence among species partners is greater in these areas.

Acknowledgments

We thank F. Salimena and L. Menini (Leopoldo Krieger Herbarium) for support in the identiication of the botanical material and E. Giannotti for the identiication of social wasp species and two anonymous referees for helpful remarks in an early version of this manuscript. We also wish to acknowledge the Coordenação de Aperfeiçoamento Pes-soal de Nível Superior (CAPES) (M.A. Clemente: doctoral fellowship), and the Conselho Nacional de Desenvolvimento Cientíico e Tecnológico (CNPq) (D. Lange 160012/2012-0; W. Dáttilo 237339/2012-9; K. Del-Claro 476074/2008-8, 472046/2011-0, and 301248/2009-5) for inancial support, and the Instituto Estadual de Floresta de Minas Gerais (IEF/MG) for logistical support.

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This aricle has supplementary material that can be down-loaded in electronic format (data set spreadsheet).

Appendix 1. Interacion matrix between social wasps-lowers

DOI: 10.13102/sociobiology.v60i3.337-344.s183

URL: htp://periodicos.uefs.br/ojs/index.php/sociobiology/rt/suppFiles/195/0